Study of male–mediated gene flow across a hybrid zone in the common shrew (Sorex araneus) using Y chromosome

CompCytogen | I (2):421—430 (2017) COMPARATIVE A reerrerewet open-access over

doi: 10.3897/CompCytogen.v | 1i2.13494 Kan Cyto genetics

http://compcytogen.pensoft.net International journal of Plant & Animal Cytogenetics,

Karyosystematics, and Molecular Systematics

Study of male—mediated gene flow across a hybrid
zone in the common shrew (Sorex araneus)
using Y chromosome

Andrei V. Polyakov', Viktor V. Panov*

| Institute of Cytology and Genetics, the Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia
2 Institute of Systematics and Ecology of Animals, the Siberian Branch of the Russian Academy of Sciences,
Novosibirsk, Russia

Corresponding author: Andrei Polyakov (polyakov@bionet.nsc.ru)

Academic editor: Jan Zima | Received 1 May 2017 | Accepted 22 May 2017 | Published 19 June 2017
http://zoobank.ore!4D6BB777-7C07-4074-9B3E-976D77C2D67F

Citation: Polyakov AV, Panov VV (2017) Study of male—mediated gene flow across a hybrid zone in the common
shrew (Sorex araneus) using Y chromosome. Comparative Cytogenetics 11(2): 421-430. https://doi.org/10.3897/
CompCytogen.v1 1i2.13494

Abstract

Despite many studies, the impact of chromosome rearrangements on gene flow between chromosome
races of the common shrew (Sorex araneus Linnaeus, 1758) remains unclear. Interracial hybrids form
meiotic chromosome complexes that are associated with reduced fertility. Nevertheless comprehensive
investigations of autosomal and mitochondrial markers revealed weak or no barrier to gene flow between
chromosomally divergent populations.

In a narrow zone of contact between the Novosibirsk and Tomsk races hybrids are produced with
extraordinarily complex configurations at meiosis I. Microsatellite markers have not revealed any barrier
to gene flow, but the phenotypic differentiation between races is greater than may be expected if gene flow
was unrestricted. To explore this contradiction we analyzed the distribution of the Y chromosome SNP
markers within this hybrid zone. The Y chromosome variants in combination with race specific autosome
complements allow backcrosses to be distinguished and their proportion among individuals within the
hybrid zone to be evaluated. The balanced ratio of the Y variants observed among the pure race individuals
as well as backcrosses reveals no male mediated barrier to gene flow. The impact of reproductive unfit-
ness of backcrosses on gene flow is discussed as a possible mechanism of the preservation of race-specific

morphology within the hybrid zone.

Keywords

Sorex araneus, phenotypic evolution, hybrid zone, gene flow, Y chromosome

Copyright Andrei V. Polyakov, Viktor V. Panov. This is an open access article distributed under the terms of the Creative Commons Attribution License
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422 Andrei V. Polyakov & Viktor V. Panov / Comparative Cytogenetics 1 1(2): 421-430 (2017)

Introduction

The common shrew (Sorex araneus Linnaeus, 1758) is assumed to be a promising mod-
el species for evolutionary studies because of the remarkable diversity of its karyotype.
Ten chromosome arms joined together in various Robertsonian fusions form dozens of
chromosome races (Wojcik et al. 2003) — “groups of geographically contiguous popu-
lations that share the same set of metacentrics and acrocentrics by descent” (Hausser
et al. 1994). Ranges of the races do not overlap but parapatric races can establish geo-
graphic contacts in narrow zones of intergradation where they hybridize and produce
interracial hybrids. At meiosis I of these hybrids, chromosomes form multivalents of
different complexity following the pattern of arm homology. These multivalents are
associated with reduced fertility of hybrids due to aberrations in chromosome pair-
ing, recombination and segregation, which in turn may lead to germ cell death or/
and generation of unbalanced gametes (Searle 1993). The decline in fertility can act
as a mechanism to impede gene flow, contributing, thus, to speciation (King 1993).
Nevertheless, comprehensive studies of protein, autosomal and mitochondrial DNA
markers revealed weak or no divergence between chromosomally divergent popula-
tions [(Wéojcik et al. 2002 (for review of previous works), Andersson et al. 2004, 2005,
Jadwiszczak et al. 2006, Lundqvist et al. 2011, Moska et al. 2011, Horn et al. 2012)].
However, in some rare cases races inhabiting adjacent areas exhibit clear morphologi-
cal distinction within the zones of intergradation (Chetnicki et al. 1996, Polyakov et
al. 2002, Polly et al. 2013), providing an excellent opportunity to clarify the details of
interracial contact.

The Novosibirsk and Tomsk races occupy the whole territory of West Siberia (Pol-
yakov et al. 1996, 2000) and form there a hybrid zone approximately 8.5 kilometers
in width (Polyakov et al. 2011). Characteristic chromosomes of the Novosibirsk race
comprise six metacentric autosomes go, hn, ik, jl, mp, qr, whereas the Tomsk race is char-
acterized by metacentrics gk, hi, jl, mn and acrocentrics 9, p, g, r. An italicized letter of
the alphabet indicates here a chromosome arm, which can either be unattached as an ac-
rocentric or attached to another chromosome arm as a metacentric (Searle et al. 1991).

Interracial hybrids form a complex multivalent (a chain of nine chromosomes) 0/
og/¢gk/kilih/hn/nm/mp/p (Polyakov et al. 2004) that is expected to cause substantially re-
duced fertility compared to pure race individuals. This assumption is supported by the
observation of a wide variety of chromosome pairing abnormalities in hybrid males, in
which the overall proportion of cells with synaptic abnormalities was 13 times higher
than in homozygotes (Borodin 2008).

The Novosibirsk and Tomsk races apparently evolved in allopatry during the last
glacial maximum in Ural and Altai refugia, respectively (Polyakov et al. 2003). They are
well differentiated for morphological traits (Yudin 1989) and DNA markers (Polyakov
et al. 2009). Interracial differences in morphology remain significant even within

the zone where races meet and hybridize (Polyakov et al. 2002, Polly et al. 2013).
The estimated duration of hybridization is at least several hundreds of generations

Y chromosome in shrew hybrid zone 423

(Polyakov et al. 2011) and preservation of race-specific morphological features within
the hybrid zone for such a long period would only be possible if the barrier to gene
flow between populations is very strong (Polly et al. 2013). If this barrier arises due to
the influence of chromosomal rearrangements on fertility of hybrids, the fecundity of
these hybrids should be very low.

Surprisingly, analysis of microsatellites has revealed low level of differentiation
within this hybrid zone, which implies a free flow of genes (Horn et al. 2012). This
contradicts the results of morphological studies and requires an additional considera-
tion. It is necessary to mention however, that analysis based on microsatellites may
underestimate the values of differentiation because of high variability of these markers
(Balloux et al. 2000).

To explore the contradiction between the microsatellites and morphology, it might
be useful to re-examine the fertility of hybrids with an additional set of markers. If
their reproductive potential is low enough to impede the introgression of morphologi-
cal traits, then microsatellites can be considered an inappropriate marker system for
such analyses. The impact of chromosome rearrangements on gene flow in this case will
be proved. Otherwise, the mechanism of restriction of gene flow needs to be revised.

In order to estimate a contribution of males - hybrids F1 in reproduction we identi-
fied two variants of a new SNP marker in the Y chromosome intron UTY11 and exam-
ined their frequencies within the hybrid zone and at the adjacent territory of the Novo-
sibirsk race. In this article we focus particularly on descendants of the hybrid males. The
Y chromosome variants in combination with race specific autosome complements allow
backcrosses to be distinguished, i.e. individuals that have the Y chromosome from one
race together with autosome complement of another parental race. This combination
can only occur if the Y chromosome is transmitted through the F1 male. ‘This study is
the first that examines the fitness of hybrids directly according to the presence of their
descendants in population. All previous studies were based on the assessment of the level
of meiotic aberrations and the width of the zones of introgression.

The methodological approach of the presented study was based on the following
reasoning:

1. Balanced gametes in hybrids have either the full Novosibirsk or the full Tomsk
complement of autosomes. Therefore, only three variants of karyotype - Novosi-
birsk homozygotes, Tomsk homozygotes and Novosibirsk/Tomsk heterozygotes,
occur within the hybrid zone.

2. The Y chromosome does not recombine and thus its alleles retain their racial
specificity.

3. AY chromosome allele of one race can occur in another race only if it has been
transmitted through the F1 male.

If the fertility of hybrids is so low that provides a barrier to gene flow, the expected
number of backcrosses will be close to zero.

424 Andrei V. Polyakov & Viktor V. Panov / Comparative Cytogenetics 1 1(2): 421-430 (2017)

Material and methods

The variability of intron UTY11 of the Y-chromosome was studied among 39 males
from the centre of the hybrid zone between the Novosibirsk and Tomsk chromosome
races of the common shrew (Figure 1). Of these males, 25 were homozygous for the
Novosibirsk race and 14 for the Tomsk race chromosome complements. Trapping and
karyotyping were performed in previous studies (Polyakov et al. 2011). Additional
32 individuals from two localities situated within the distribution range of the No-
vosibirsk race (27 from Akademgorodok and 5 from Chemskoy Bor) were examined.
Shrews of these localities are monomorphic for the Novosibirsk race karyotypes (Kral
and Radjabli 1974, Polyakov et al. 1997).

Intron UTY11 of the Y chromosome was amplified following the protocol of
Hellborg and Ellegren (2003). Sequencing was performed in both directions and ana-
lyzed using an ABI Prism 3100 genetic analyzer (Applied Biosystems) in the SB RAS
Genomics Core Facility (Novosibirsk, Russia).

Student's t-test statistics was used to assess the difference in the ratio of the Y hap-
lotypes between races. The level of linkage disequilibrium between the Y haplotypes
(Y) and autosome complements (A) was quantified by the coefficient of linkage dis-
equilibrium D,, = p,, — PyPa:

Results

Two haplotypes of intron UTY11 with cytosine/thymine substitution at position 585
(C-haplotype/T-haplotype, respectively) were identified among the studied shrews
(GenBank (www.ncbi.nlm.nih.gov/Genbank) accession numbers KY652093 and
KY652094). Table 1 shows the distribution of these haplotypes in the studied races.
The haplotype C was detected in the shrews trapped in Akademgorodok, Chemskoy
Bor and in the hybrid zone. The haplotype T was detected in the hybrid zone only.

In the hybrid zone the frequency of C-haplotype (0.77) is greater than the frequency of
T-haplotype (0.23), however the ratio of the Y haplotypes between shrews with the Novo-
sibirsk and Tomsk autosome complements does not differ statistically (t,= 0.59, P > 0.05).

We did not detect linkage disequilibrium between the Novosibirsk- and Tomsk-
derived autosomes and the Y chromosome variants (D = 0.02, y2 = 0.37, P > 0.05).

Table |. Frequency of the Y chromosome variants in the studied races.

Localities Frequency of T-haplotype | SE
Novosibirsk 0.08
Hybrid zone 0.29 0.12
0.23 0.07
Akademgorodok Novosibirsk
Chemskoy Bor Novosibirsk

Total

Y chromosome in shrew hybrid zone 425

Novosibirsk race
area

- , Akademgorodok

Longitude

Figure |. Location of sampling sites. Dotted line marks limits of introgression of the Tomsk autosomes

complement; firm curved line determines the centre of the hybrid zone according to Polyakov et al. (2011).

Discussion

Akademgorodok and Chemskoy Bor are situated within the distribution range of
the Novosibirsk race. Only the C-haplotype of the Y chromosome was found among
shrews from both localities. Thus, we may suggest that the Novosibirsk race is mono-
morphic for this haplotype.

In the hybrid zone the frequency of C-haplotype is greater than the frequency of
T-haplotype. This may indicate that both haplotypes of the Y chromosome are present
in the Tomsk race. Alternatively, this could reflect a shift of the Y-chromosomal cline
towards the Tomsk race area. The latter explanation is consistent with the results of
previous morphological studies, where the clines in medial and lateral mandible sizes
were centered at the Tomsk race side of the hybrid zone (Polly et al. 2013).

Backcrosses with the T-haplotype and autosomes of the Novosibirsk race are present
in the hybrid zone. They would not be there, if the hybrid males were sterile. Nearly
equal number of the T-haplotype in combination with both autosome complements
implies a continuous flow of Y chromosome from the Tomsk to Novosibirsk race. This
observation suggests that even if the hybrid males suffer from reduced fertility, it does
not provide an insurmountable barrier to gene flow between the contacting populations.

Hybridization between divergent populations begins with the production of F1
and subsequent backcrossing. Repeated generations of backcross individuals result in
introgression of mutations, collected by populations in allopatry (Maheshwari and
Barbash 2011). Introgression can be prevented if hybrid incompatibilities reduce the
fitness of the F1 or/and backcross generations (Turelli and Orr 2000).

Poor reproductive performance of hybrid shrews with chromosomal multivalents
can be related not only to aberrations in generative tissues and gametes. The other cause
can be the failure in competition for mating or low viability of their offspring. Our
results indicate that none of this happens and the F1 hybrids are adequately involved
in reproduction. The balanced ratio of Y variants among the pure race individuals and
backcrosses in the Novosibirsk/Tomsk hybrid zone suggests that the F1 produce viable

426 Andrei V. Polyakov & Viktor V. Panov / Comparative Cytogenetics 1 1(2): 421-430 (2017)

progeny. It does not explain the distinct differentiation of shrews in morphological
traits. However, if this differentiation is facilitated by a barrier to gene flow, and if this
barrier is determined by hybrid incompatibilities, the results of the present study make
the list of possible incompatibilities shorter. Indeed, after the rehabilitation of the F1,
low fertility of backcrosses remains the only thing that can be suspected to influence
gene flow. Certainly, this assumption requires careful consideration. Below we discuss
some issues related to the possible impact of low fertility of backcrosses on gene flow.
The inheritance of morphological traits is defined by many loci with additive effect
(Kemper et al. 2012). In a study of the inheritance of body size, crosses between strains
of laboratory mice with different size have been made. In these experiments the F1
and F2 means were halfway between the parents and the backcross means were half-
way between the F1 and respective parents (Butler 1952, Chai 1956). Similar crosses
occur among shrews within the hybrid zone. In evaluation of morphological traits of
shrews with consideration of their karyotypes, all the homozygous individuals with the
Novosibirsk race karyotype were significantly smaller than the Tomsk homozygous in-
dividuals (Polyakov et al. 2002). This difference enabled differentiation of two separate
morphotype groups, and the Novosibirsk shrews never grouped with the Tomsk shrews
and vice-versa (see Figure 1 in Polyakov et al. 2002). Morphological variability of the
heterozygotes was much broader and overlapped the extent of variation found in both
homozygotes. Figure 2 illustrates the segregation of morphology and karyotypes in
the hybrid zone as it may be expected following the experiments of Butler (1952) and
Chai (1956). In this figure the relationship between the karyotypes and morphological
types at stages the F1 and the first-generation backcrosses is in a good agreement with
the experimental data from the hybrid zone of shrews. Parents and homozygous first-
generation backcrosses form two distinct morphological groups, while karyotypically
similar Fl and heterozygous first-generation backcrosses show variation that overlaps
both homozygous groups. The appearance of the second-generation backcrosses, that
combine the homozygous karyotypes of one race with a morphotype of the other race,
would bring discrepancy in this concordance. However, no discrepancy between the
karyotypes and morphological types was observed in experimental studies of the No-
vosibirsk/Tomsk hybrid zone, and it can be assumed that the second-generation back-
crosses do not appear in this case. The reason of the absence of the second-generation
backcrosses is difficult to explain unequivocally. We can only assume that if the first-
generation backcrosses had been involved in reproduction, unlimited introgression
could have been expected: foreign alleles would have accumulated on both sides of the
hybrid zone and phenotypic differences would have become blurred after several gen-
erations. However, although hybridization between the Novosibirsk and Tomsk races
has been lasting for much longer than several generations, none of this has happened.
Even a strong barrier to gene flow, based on low fertility of backcrosses, is not incom-
patible with the lack of differentiation of the autosomal markers including microsatel-
lites. The populations in contact may have clear differentiation for these markers outside
of the hybrid zone. If the sampling is carried out in the zone of hybridization, backcrosses
will be collected together with pure race specimens. Recombination in the F1 shufHes

Y chromosome in shrew hybrid zone 427

Population | morphotype Population 2 morphotype

Figure 2. Segregation of karyotypes and morphological traits in the hybrid zone between two chromo-
some races. Positions of karyotypes reflect their morphological state: individuals of pure parental type (P1
and P2) with the most pronounced morphological differences occupy rightmost and leftmost positions,
F1 — intermediate between P1 and P2 and the first-generation backcrosses — intermediate between F1 and
respective parents (B1,, and B1,,,). The second-generation backcrosses (B2) contain karyotypes that do
not correspond to the expected morphotypes (marked with squared frames). Round frames mark karyo-

typically indistinguishable parents, Fl and B1 (see text for details).

mutations between the race specific chromosome complements and backcrosses inherit
alleles from both races. The karyotypes of homozygous backcrosses are indistinguishable
from the karyotypes of the pure race individuals. Appearance of these backcrosses in the
same group with the pure race individuals may significantly reduce the observed dif-
ferentiation. Evaluation of samples collected within the zone of hybridization may thus
explain the failure of previous studies to demonstrate a distinct differentiation.

Low reproductive ability of the generation following the F1 can become a promis-
ing hypothesis for further studies of barriers to gene flow between the chromosome
races of the common shrew.

Conclusion

Aberrations in pairing, recombination and segregation of chromosomes in hybrids with
complex meiotic configurations are a generally assumed barrier to gene flow among the

428 Andrei V. Polyakov & Viktor V. Panov / Comparative Cytogenetics 1 1(2): 421-430 (2017)

karyotypically divergent chromosome races of the common shrew (Searle 1993). The
presented study suggests that gene incompatibilities in backcrosses may have more sub-
stantial influence on gene flow than erroneous behaviour of chromosomes at meiosis.
Apparently, the Novosibirsk and Tomsk races have not yet reached the final stage of
divergence, when hybridization does not go beyond the F1 production; however, the
poor reproductive performance of the first-generation backcrosses may preserve the
adaptive genetic architecture from assimilation and thus contribute to further diver-
gence, promoting the progress of speciation.

Acknowledgments

We are grateful to Jan Zima and anonymous referee for the valuable comments made
on the manuscript. This work was supported by the RF Basic Project No. 0324-2015-
0004 and research grant from Russian Foundation for Basic Research Ne 13-04-003 16.

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